Making bigger brains–the evolution of neural-progenitor-cell division

Fish, Jennifer L.; Dehay, Colette; Kennedy, Henry; Huttner, Wieland B.

doi:10.1242/jcs.023465

Cited by 255 publications

(250 citation statements)

References 77 publications

Supporting

Mentioning

232

Contrasting

Order By: Relevance

“…Our data imply that the same principal machinery (actomyosin) and cell biological process (constriction of the entire apical process) are responsible for 2 hallmarks of CNS development, the pseudostratification of the VZ, which increases in vertebrate evolution (5,27), and the generation of a second neurogenic progenitor layer basal to the VZ, the SVZ, which is characteristic of the mammalian telencephalon (28). Interestingly, an increase in the SVZ is thought to underly cortical expansion (8,(27)(28)(29), and the major type of primate SVZ progenitor has been proposed to retain certain features of APs (8,27). Given these considerations, and our findings showing that the ap3bl nuclear translocation in the course of SVZ formation is highly related to the ap3bl leg of INM of VZ progenitors, the actomyosin machinery determining the extent of ap3bl nuclear translocation is likely to be a key target of evolutionary change.…”

Section: Basal-to-apical Nuclear Migration Versus Apical-to-basal Nucmentioning

confidence: 71%

See 1 more Smart Citation

Myosin II is required for interkinetic nuclear migration of neural progenitors

Schenk

Wilsch‐Bräuninger

Calegari

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

147

151

View full text Add to dashboard Cite

Interkinetic nuclear migration (INM) is a hallmark of the polarized stem and progenitor cells in the ventricular zone (VZ) of the developing vertebrate CNS. INM is responsible for the pseudostratification of the VZ, a crucial aspect of brain evolution. The nuclear migration toward the apical centrosomes in G2 is thought to be a dyneinmicrotubule-based process. By contrast, the cytoskeletal machinery involved in the basally directed nuclear translocation away from the centrosome in G1 has been enigmatic. Studying the latter aspect of INM requires manipulation of the cytoskeleton without impairing mitosis and cytokinesis. To this end, we have established a culture system of mouse embryonic telencephalon that reproduces cortical development, and have applied it to explore a role of actomyosin in INM. Using the nonmuscle myosin II inhibitor blebbistatin at a low concentration at which neither cell cycle progression nor cytokinesis is impaired, we show that myosin II is required for the apical-to-basal (ap3bl), ab-centrosomal INM. Myosin II activity is also necessary for the nuclear translocation during delamination of subventricular zone (SVZ) cells, a second, telencephalon-specific type of neural progenitor. Moreover, the inhibition of ab-centrosomal INM changes the balance between VZ and SVZ progenitor cell fate. Our data suggest a unifying concept in which the actomyosin contraction underlying ab-centrosomal INM sets the stage for the evolutionary increase in VZ pseudostratification and for SVZ progenitor delamination, a key process in cortical expansion.cell cycle ͉ cerebral cortex ͉ cytoskeleton ͉ neural stem cells ͉ neurogenesis

show abstract

Section: Basal-to-apical Nuclear Migration Versus Apical-to-basal Nucmentioning

confidence: 71%

“…Importantly, by moving the interphase nuclei of APs away from the apical surface, the apical-to-basal (ap3bl) leg of INM during G1 serves to reserve the apical space for mitosis, and thereby promotes the expansion of APs (see ref. 8 …”

mentioning

confidence: 99%

Myosin II is required for interkinetic nuclear migration of neural progenitors

Schenk

Wilsch‐Bräuninger

Calegari

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

147

151

View full text Add to dashboard Cite

show abstract

“…Although many intrinsic and extrinsic factors may influence cortical size and cytoarchitecture, such as patterns of neuronal migration (Letinic et al, 2002;Kriegstein and Noctor, 2004;Bystron et al, 2006), thalamic afferents (Windrem and Finlay, 1991;Dehay et al, 2001) and the diversification of subventricular zone neural progenitors (Smart et al, 2002;Haubensak et al, 2004;Miyata et al, 2004;Noctor et al, 2004;Fish et al, 2008), an increase in neuron number during brain development and evolution is ultimately controlled by the number and modes of division of neural progenitors in the embryonic ventricular and subventricular zones (Götz and Huttner, 2005;Kriegstein et al, 2006;Fish et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…On a progenitor cell-intrinsic level, features such as apical-basal polarity, mitotic spindle orientation and cell cycle length are involved in shifting progenitors from proliferation to differentiation, and thus influence cortical size (Bond and Woods, 2006;Buchman and Tsai, 2007;Dehay and Kennedy, 2007;Farkas and Huttner, 2008;Fish et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors

Pulvers

Huttner

2009

Development

Self Cite

View full text Add to dashboard Cite

The extent of apoptosis of neural progenitors is known to influence the size of the cerebral cortex. Mouse embryos lacking Brca1, the ortholog of the human breast cancer susceptibility gene BRCA1, show apoptosis in the neural tube, but the consequences of this for brain development have not been studied. Here we investigated the role of Brca1 during mouse embryonic cortical development by deleting floxed Brca1 using Emx1-Cre, which leads to conditional gene ablation specifically in the dorsal telencephalon after embryonic day (E) 9.5. The postnatal Brca1-ablated cerebral cortex was substantially reduced in size with regard to both cortical thickness and surface area. Remarkably, although the thickness of the cortical layers (except for the upper-most layer) was decreased, cortical layering as such was essentially unperturbed. High levels of apoptosis were found at E11.5 and E13.5, but dropped to near-control levels by E16.5. The apoptosis at the early stage of neurogenesis occurred in both BrdU pulse-labeled neural progenitors and the neurons derived therefrom. No changes were observed in the mitotic index of apical (neuroepithelial, radial glial) progenitors and basal (intermediate) progenitors, indicating that Brca1 ablation did not affect cell cycle progression. Brca1 ablation did, however, result in the nuclear translocation of p53 in neural progenitors, suggesting that their apoptosis involved activation of the p53 pathway. Our results show that Brca1 is required for the cerebral cortex to develop to normal size by preventing the apoptosis of early cortical progenitors and their immediate progeny. Development 136, 1859Development 136, -1868Development 136, (2009Development 136, ) doi:10.1242 Max Planck Institute for Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany. . Brca1 is widely expressed in proliferating tissues and is also expressed in the ventricular neuroepithelium of the neural tube (Korhonen et al., 2003). KEY WORDS: Brca1, Apoptosis, Cerebral cortexThe relevance of apoptosis in cortical development (Haydar et al., 1999), the increased apoptosis of neuroepithelial cells observed in systemic Brca1 knockouts (Gowen et al., 1996;Xu et al., 2001), and the expression pattern of Brca1 in neural progenitors, when considered together, raise the intriguing possibility that Brca1 might have a role in the development of the cerebral cortex. Moreover, the apparent link between BRCA1 and the primary microcephaly genes ASPM (Bond et al., 2002;Zhong et al., 2005) and MCPH1 (Xu et al., 2004;Lin et al., 2005), whereby knockdown of either microcephaly gene leads to a decrease in BRCA1 levels, also leads to the question of whether BRCA1 has a role in brain size regulation. In this context, it is interesting to note that BRCA1 has undergone positive selection in the primate lineage (Huttley et al., 2000), raising the possibility that it might have been selected owing to a function in brain development. Here, we have investigated this issue by conditional ablation of Brca1 in cor...

show abstract

“…In many mammalian species, this area is progressively subdivided into two subregions, the inner subventricular zone (ISVZ) and the outer subventricular zone (OSVZ), which appears later in development and is greatly expanded in gyrencephalic species (Cheung et al, 2007; Fish et al, 2008; Franco and Muller, 2013; Kriegstein et al, 2006; Lui et al, 2011; Martinez‐Cerdeno et al, 2012; Smart et al, 2002). The SVZ harbors a variety of neural progenitors, collectively referred to as basal progenitors, which eventually become the main source of neocortical neurons.…”

mentioning

confidence: 99%

S‐phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex

García

Chang

Arai

et al. 2015

J of Comparative Neurology

Self Cite

View full text Add to dashboard Cite

The evolutionary expansion of the neocortex primarily reflects increases in abundance and proliferative capacity of cortical progenitors and in the length of the neurogenic period during development. Cell cycle parameters of neocortical progenitors are an important determinant of cortical development. The ferret (Mustela putorius furo), a gyrencephalic mammal, has gained increasing importance as a model for studying corticogenesis. Here, we have studied the abundance, proliferation, and cell cycle parameters of different neural progenitor types, defined by their differential expression of the transcription factors Pax6 and Tbr2, in the various germinal zones of developing ferret neocortex. We focused our analyses on postnatal day 1, a late stage of cortical neurogenesis when upper‐layer neurons are produced. Based on cumulative 5‐ethynyl‐2′‐deoxyuridine (EdU) labeling as well as Ki67 and proliferating cell nuclear antigen (PCNA) immunofluorescence, we determined the duration of the various cell cycle phases of the different neocortical progenitor subpopulations. Ferret neocortical progenitors were found to exhibit longer cell cycles than those of rodents and little variation in the duration of G1 among distinct progenitor types, also in contrast to rodents. Remarkably, the main difference in cell cycle parameters among the various progenitor types was the duration of S‐phase, which became shorter as progenitors progressively changed transcription factor expression from patterns characteristic of self‐renewal to those of neuron production. Hence, S‐phase duration emerges as major target of cell cycle regulation in cortical progenitors of this gyrencephalic mammal. J. Comp. Neurol. 524:456–470, 2016. © 2015 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

show abstract

Making bigger brains–the evolution of neural-progenitor-cell division

Cited by 255 publications

References 77 publications

Myosin II is required for interkinetic nuclear migration of neural progenitors

Myosin II is required for interkinetic nuclear migration of neural progenitors

Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors

S‐phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex

Contact Info

Product

Resources

About